Natural Product Sciences

The Korean Society of Pharmacognosy (한국생약학회)
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Hyperoside Protects Cells against Gamma Ray Radiation-Induced Apoptosis in Hamster Lung Fibroblast

  • Piao, Mei Jing (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Kim, Ki Cheon (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Cho, Suk Ju (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University) ;
  • Chae, Sungwook (Aging Research Center, Korea Institute of Oriental Medicine) ;
  • Kang, Sam Sik (Natural Products Research Institute and College of Pharmacy, Seoul National University) ;
  • Hyun, Jin Won (School of Medicine and Institute for Nuclear Science and Technology, Jeju National University)
  • Received : 2013.03.27
  • Accepted : 2013.06.02
  • Published : 2013.06.30
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Abstract

Ionizing radiation, including that evoked by gamma (${\gamma}$)-rays, induces oxidative stress through the generation of reactive oxygen species, resulting in apoptosis, or programmed cell death. This study aimed to elucidate the radioprotective effects of hyperoside (quercetin-3-O-galactoside) against ${\gamma}$-ray radiation-induced apoptosis in Chinese hamster lung fibroblasts, V79-4 and demonstrated that the compound reduced levels of intracellular reactive oxygen species in ${\gamma}$-ray-irradiated cells. Hyperoside also protected irradiated cells against DNA damage (evidenced by pronounced DNA tails and elevated phospho-histone H2AX and 8-oxoguanine content) and membrane lipid peroxidation. Furthermore, hyperoside prevented the ${\gamma}$-ray-provoked reduction in cell viability via the inhibition of apoptosis through the increased levels of Bcl-2, the decreased levels of Bax and cytosolic cytochrome c, and the decrease of the active caspase 9 and caspase 3 expression. Taken together, these results suggest that hyperoside defend cells against ${\gamma}$-ray radiation-induced apoptosis by inhibiting oxidative stress.

Keywords

References

  1. Afaq, F. and Mukhtar, H., Botanical antioxidants in the prevention of photocarcinogenesis and photoaging. Exp. Dermatol. 15, 678-684 (2006). https://doi.org/10.1111/j.1600-0625.2006.00466.x
  2. Bhosle, S.M., Huilgol, N.G., and Mishra, K.P., Enhancement of radiationinduced oxidative stress and cytotoxicity in tumor cells by ellagic acid. Clin. Chim. Acta 359, 89-100 (2005). https://doi.org/10.1016/j.cccn.2005.03.037
  3. Bouhlel, I., Valenti, K., Kilani, S., Skandrani, I., Ben Sghaier, M., Mariotte, A.M., Dijoux-Franca, M.G., Ghedira, K., Hininger-Favier, I., Laporte, F., and Chekir-Ghedira, L., Antimutagenic, antigenotoxic and antioxidant activities of Acacia salicina extracts (ASE) and modulation of cell gene expression by $H_{2}O_{2}$ and ASE treatment. Toxicol. In Vitro 22, 1264-1272 (2008). https://doi.org/10.1016/j.tiv.2008.04.008
  4. Bonner, W.M., Redon, C.E., Dickey, J.S., Nakamura, A.J., Sedelnikova, O.A., Solier, S., and Pommier, Y., Gamma H2AX and cancer. Nat. Rev. Cancer 8, 957-967 (2008). https://doi.org/10.1038/nrc2523
  5. Carmichael, J., DeGraff, W.G., Gazdar, A.F., Minna, J.D., and Mitchell, J.B., Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res. 47, 936-941 (1987).
  6. Chen, L., Li, J., Luo, C., Liu, H., Xu, W., Chen, G., Liew, O. W., Zhu, W., Puah, C. M., Shen, X., and Jiang, H., Binding interaction of quercetin-3-beta-galactoside and its synthetic derivatives with SARS-CoV 3CL(pro): structure-activity relationship studies reveal salient pharmacophore features. Bioorg. Med. Chem. 14, 8295-8306 (2006). https://doi.org/10.1016/j.bmc.2006.09.014
  7. Choi, K.M., Kang, C.M., Cho, E.S., Kang, S.M., Lee, S.B., and Um, H.D., Ionizing radiationinduced micronucleus formation is mediated by reactive oxygen species that are produced in a manner dependent on mitochondria, Nox1, and JNK. Oncol. Rep. 17, 1183-1188 (2007).
  8. Dizdaroglu, M., Jaruga, P., Birincioglu, M., and Rodriguez, H., Free radical-induced damage to DNA: mechanisms and measurement. Free Radic. Biol. Med. 32, 1102-1115 (2002). https://doi.org/10.1016/S0891-5849(02)00826-2
  9. Ferguson, L.R., Role of plant polyphenols in genomic stability. Mutat. Res. 475, 89-111 (2001). https://doi.org/10.1016/S0027-5107(01)00073-2
  10. Gao, K., Henning, S.M., Niu, Y., Youssefian, A.A., Seeram, N.P., Xu, A., and Heber, D., The citrus flavonoid naringenin stimulates DNA repair in prostate cancer cells. J. Nutr. Biochem. 17, 89-95 (2006). https://doi.org/10.1016/j.jnutbio.2005.05.009
  11. Guarrera, S., Sacerdote, C., Fiorini, L., Marsala, R., Polidoro, S., Gamberini, S., Saletta, F., Malaveille, C., Talaska, G., Vineis, P., and Matullo, G., Expression of DNA repair and metabolic genes in response to a flavonoid-rich diet. Br. J. Nutr. 98, 525-533 (2007). https://doi.org/10.1017/S0007114507725151
  12. Jagetia, A., Jagetia, G.C., and Jha, S., Naringin, a grapefruit flavanone, protects V79 cells against the bleomycin-induced genotoxicity and decline in survival. J. Appl. Toxicol. 27, 122-132 (2007). https://doi.org/10.1002/jat.1175
  13. Kim, S.Y., Seo, M., Oh, J.M., Cho, E.A., and Juhnn, Y.S., Inhibition of gamma ray-induced apoptosis by stimulatory heterotrimeric GTP binding protein involves Bcl-xL downregulation in SH-SY5Y human neuroblastoma cells. Exp. Mol. Med. 39, 583-593 (2007). https://doi.org/10.1038/emm.2007.64
  14. Landes, T., and Martinou, J.C., Mitochondrial outer membrane permeabilization during apoptosis: the role of mitochondrial fission. Biochim. Biophys. Acta 1813, 540-545 (2011). https://doi.org/10.1016/j.bbamcr.2011.01.021
  15. Lee, J.H., Kim, S.Y., Kil, I.S., and Park, J.W., Regulation of ionizing radiation-induced apoptosis by mitochondrial NADP+-dependent isocitrate dehydrogenase. J. Biol. Chem. 282, 13385-13394 (2007). https://doi.org/10.1074/jbc.M700303200
  16. Lee, S.Y., Kim, J.S., and Kang, S.S., Flavonol glycosides from the aerial parts of Metaplexis japonica. Kor. J. Pharmacogn. 43, 206-212 (2012).
  17. Li, S., Zhang, Z., Cain, A., Wang, B., Long, M., and Taylor, J., Antifungal activity of camptothecin, trifolin, and hyperoside isolated from Camptotheca acuminata. J. Agric. Food Chem. 53, 32-37 (2005). https://doi.org/10.1021/jf0484780
  18. Lin, X., Zhang, F., Bradbury, C.M., Kaushal, A., Li, L., Spitz, D.R., Aft, R.L., and Gius, D., 2-Deoxy-D-glucose-induced cytotoxicity and radiosensitization in tumor cells is mediated via disruptions in thiol metabolism. Cancer Res. 63, 3413-3417 (2003).
  19. Liu, Y. and Luo, W., Betulinic acid induces Bax/Bak-independent cytochrome c release in human nasopharyngeal carcinoma cells. Mol. Cells 33, 517-524 (2012). https://doi.org/10.1007/s10059-012-0022-5
  20. Liu, Z., Tao, X., Zhang, C., Lu, Y., and Wei, D., Protective effects of hyperoside (quercetin-3-o-galactoside) to PC12 cells against cytotoxicity induced by hydrogen peroxide and tert-butyl hydroperoxide. Biomed. Pharmacother. 59, 481-490 (2005). https://doi.org/10.1016/j.biopha.2005.06.009
  21. Luo, L., Sun, Q., Mao, Y.Y., Lu, Y.H., and Tan, R.X., Inhibitory effects of flavonoids from Hypericum perforatum on nitric oxide synthase. J. Ethnopharmacol. 93, 221-225 (2004). https://doi.org/10.1016/j.jep.2004.03.042
  22. Middleton, E.Jr., Kandaswami, C., and Theoharides, T.C., The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol. Rev. 52, 673-751 (2000).
  23. Nicoletti, I., Migliorati, G., Pagliacci, M.C., Grignani, F., and Riccardi, C., A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139, 271-279 (1991). https://doi.org/10.1016/0022-1759(91)90198-O
  24. Nijveldt, R.J., van Nood, E., van Hoorn, D.E., Boelens, P.G., van Norren, K., and van Leeuwen, P.A., Flavonoids: a review of probable mechanisms of action and potential applications. Am. J. Clin. Nutr. 74, 418-425 (2001).
  25. Okimoto, Y., Watanabe, A., Niki, E., Yamashita, T., and Noguchi, N., A novel fluorescent probe diphenyl-1-pyrenylphosphine to follow lipid peroxidation in cell membranes. FEBS Lett. 474, 137-140 (2000). https://doi.org/10.1016/S0014-5793(00)01587-8
  26. Perkins, C.L., Fang, G., Kim, C.N., and Bhalla, K.N., The role of Apaf-1, caspase-9, and bid proteins in etoposide- or paclitaxel-induced mitochondrial events during apoptosis. Cancer Res. 60, 1645-1653 (2000).
  27. Piao, M.J., Kang, K.A., Zhang, R., Ko, D.O., Wang, Z.H., You, H.J., Kim, H.S., Kim, J.S., Kang, S.S., and Hyun, J.W., Hyperoside prevents oxidative damage induced by hydrogen peroxide in lung fibroblast cells via an antioxidant effect. Biochim. Biophys. Acta 1780, 1448-1457 (2008). https://doi.org/10.1016/j.bbagen.2008.07.012
  28. Prenner, L., Sieben, A., Zeller, K., Weiser, D., and Haberlein, H., Reduction of High-Affinity beta(2)-Adrenergic Receptor Binding by Hyperforin and Hyperoside on Rat C6 Glioblastoma Cells Measured by Fluorescence Correlation Spectroscopy. Biochemistry 46, 5106-5113 (2007). https://doi.org/10.1021/bi6025819
  29. Rajagopalan, R., Ranjan, S.K., and Nair, C.K., Effect of vinblastine sulfate on gammaradiation-induced DNA single-strand breaks in murine tissues. Mutat. Res. 536, 15-25 (2003). https://doi.org/10.1016/S1383-5718(03)00015-9
  30. Renault, T.T., Teijido, O., Antonsson, B., Dejean, L.M., and Manon, S., Regulation of Bax mitochondrial localization by Bcl-2 and Bcl-x(L): keep your friends close but your enemies closer. Int. J. Biochem. Cell Biol. 45, 64-67 (2013). https://doi.org/10.1016/j.biocel.2012.09.022
  31. Rosenkranz, A.R., Schmaldienst, S., Stuhlmeier, K.M., Chen,W., Knapp,W., and Zlabinger, G.J., A microplate assay for the detection of oxidative products using 2',7'-dichlorofluorescein-diacetate. J. Immunol. Methods 156, 39-45 (1992). https://doi.org/10.1016/0022-1759(92)90008-H
  32. Sies, H., Oxidative Stress, Academic Press, New York, 1983.
  33. Tope, A.M. and Panemangalore, M., Assessment of oxidative stress due to exposure to pesticides in plasma and urine of traditional limitedresource farm workers: formation of the DNA-adduct 8-hydroxy-2-deoxy-guanosine (8-OHdG). J. Environ. Sci. Health B 42, 151-155 (2007). https://doi.org/10.1080/03601230601123276
  34. Troiano, L., Ferraresi, R., Lugli, E., Nemes, E., Roat, E., Nasi,M., Pinti, M., and Cossarizza, A., Multiparametric analysis of cells with different mitochondrial membrane potential during apoptosis by polychromatic flow cytometry. Nat. Protoc. 2, 2719-2727 (2007). https://doi.org/10.1038/nprot.2007.405
  35. Trumbeckaite, S., Bernatoniene, J., Majiene, D., Jakstas, V., Savickas, A., and Toleikis, A., The effect of flavonoids on rat heart mitochondrial function. Biomed. Pharmacother. 60, 245-248 (2006).
  36. Tuder, R.M., Zhen, L., and Cho, C.Y., Taraseviciene-Stewart, L., Kasahara, Y., Salvemini, D., Voelkel, N.F., and Flores, S.C., Oxidative stress and apoptosis interact and cause emphysema due to vascular endothelial growth factor receptor blockade. Am. J. Respir. Cell. Mol. Biol. 29, 88-97 (2003). https://doi.org/10.1165/rcmb.2002-0228OC
  37. Wu, L.L., Yang, X.B., Huang, Z.M., Liu, H.Z., and Wu, G.X., In vivo and in vitro antiviral activity of hyperoside extracted from Abelmoschus manihot (L) medik. Acta. Pharmacol. Sin. 28, 404-409 (2007). https://doi.org/10.1111/j.1745-7254.2007.00510.x
  38. Yang, P., He, X.Q., Peng, L., Li, A.P., Wang, X.R., Zhou, J.W., and Liu, Q.Z., The role of oxidative stress in hormesis induced by sodium arsenite in human embryo lung fibroblast (HELF) cellular proliferation model. J. Toxicol. Environ. Health A 70, 976-983 (2007). https://doi.org/10.1080/15287390701290832
  39. Yen, G.C., Duh, P.D., Tsai, H.L., and Huang, S.L., Pro-oxidative properties of flavonoids in human lymphocytes. Bioscience, Biotech. Biochem. 67, 1215-1222 (2003). https://doi.org/10.1271/bbb.67.1215
  40. Zhang, J., Stanley, R.A., Adaim, A., Melton, L.D., and Skinner, M.A., Free radical scavenging and cytoprotective activities of phenolic antioxidants. Mol. Nutr. Food Res. 50, 996-1005 (2006). https://doi.org/10.1002/mnfr.200600072
  41. Zou, Y., Lu, Y., and Wei, D., Antioxidant activity of a flavonoid-rich extract of Hypericum perforatum L. in vitro. J. Agric. Food Chem. 52, 5032-5039 (2004). https://doi.org/10.1021/jf049571r